(1) Epigenetic mechanisms of plant immune receptor gene expression

A main focus of research in my lab has been the Arabidopsis PHD-finger protein EDM2, which is required for race-specific plant immunity. I cloned EDM2 in summer 2003 as a post-doc in Jeff Dangl’s lab at University of North Carolina. Since 2005 we have been continuously working on this gene in my lab and found it to encode a nuclear histone binding protein that controls besides plant immune responses also several developmental processes. EDM2 executes at least some of its roles by binding to the suppressive epigenetic H3K9me2 mark in transposons closely associated with its target genes. We further found EDM2 to promote expression of at least two separate NLR-type immune receptor genes by suppressing proximal transcript termination/polyadenylation. High expression levels of these NLRs are associated with fitness costs. By profiling genome-wide effects of EDM2 we recently found it to have a broader role in controlling NLR expression. In order to mitigate fitness costs caused by its promoting effects on expression of some NLR genes, EDM2 suppresses expression of many additional members of this gene family. This way EDM2 seems to compensate for fitness penalties caused by high expression of some NLR genes by suppression of others. In this important function EDM2 is assisted by the RNA-binding protein EDM3, which we recently identified as an EDM2 interactor by map based cloning and IP-studies.

This work has been funded by the following grants from the US National Science Foundation:

NSF IOS # 6890764

NSF IOS # 1052556

NSF MCB # 1330905

NSF IOS # 1457329

We published the following papers related to this project:

- Eulgem, T., Tsuchiya, T., Wang, X.-J., Beasley, B., Cuzick, A., Tör, M., Zhu, T, McDowell, J.M., Holub, E. & Dangl, J.L. 2007, “EDM2 is a novel component of RPP7-dependent disease resistance in Arabidopsis that affects RPP7 transcript levels”. The Plant Journal, 49 (5): 829–839;

https://pubmed.ncbi.nlm.nih.gov/17253987/

- Tsuchiya T, Eulgem T. 2010, “The Arabidopsis defense component EDM2 affects the floral transition in an FLC-dependent manner”. The Plant Journal. 62: 518-28.

https://onlinelibrary.wiley.com/doi/full/10.1111/j.1365-313X.2010.04169.x

- Tsuchiya T, Eulgem T. 2010, “Co-option of EDM2 to distinct regulatory modules in Arabidopsis thaliana development”. BMC Plant Biology 10: 203.

https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2956552/

- Tsuchiya T, Eulgem T. 2011, “EMSY-like genes are required for full RPP7-mediated race specific immunity and basal defense in Arabidopsis”. Molecular Plant Microbe Interactions, 24: 1573–1581

https://pubmed.ncbi.nlm.nih.gov/21830950/

- Tokuji Tsuchiya & Thomas Eulgem. 2013, “Mutations in EDM2 selectively affect silencing states of transposons and induce plant developmental plasticity”. Scientific Reports, 3: 1701

https://www.nature.com/articles/srep01701

- Tokuji Tsuchiya & Thomas Eulgem. 2013, “An alternative polyadenylation mechanism coopted to the Arabidopsis RPP7 gene through intronic retrotransposon domestication”. Proc Natl Acad Sci USA, 110:E3535–E3543.

https://www.pnas.org/content/110/37/E3535.long

- Tokuji Tsuchiya & Thomas Eulgem. 2014, “The PHD-finger module of the Arabidopsis thaliana defense regulator EDM2 can recognize triply modified histone H3 peptides”. Plant Signal Behav. 9. pii: e29202.

https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4203584/

- Yan Lai and Thomas Eulgem, 2017, “Transcript-level expression control of plant NLR genes” Molecular Plant Pathology, DOI: 10.111/mpp.12607;

https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6638128/

- Yan Lai, Alayne Cuzick, Xueqing M. Lu, Jianqiang Wang, Neerja Katiyar, Tokuji Tsuchiya, Karine Le Roch, John M. McDowell, Eric Holub and Thomas Eulgem; 2018 “The Arabidopsis RRM domain protein EDM3 mediates race-specific disease resistance by controlling H3K9me2 dependent alternative polyadenylation of RPP7 immune receptor transcripts”, The Plant Journal 97: 646-660,

https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7138032/

- Yan Lai, Xueqing (Maggie) Lu, Josquin Daron, Songqin Pan, Jianqiang Wang, Wei Wang, Tokuji Tsuchiya, Eric Holub, John M. McDowell, R. Keith Slotkin, Karine Le Roch and Thomas Eulgem, 2020, “The Arabidopsis PHD-finger protein EDM2 has multiple roles in balancing NLR immune receptor gene expression”, PLOS Genetics,

https://doi.org/10.1371/journal.pgen.1008993;